{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T01:37:46Z","timestamp":1777426666837,"version":"3.51.4"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"1","funder":[{"DOI":"10.13039\/501100004963","name":"Seventh Framework Programme","doi-asserted-by":"publisher","award":["242095"],"award-info":[{"award-number":["242095"]}],"id":[{"id":"10.13039\/501100004963","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001713","name":"European and Developing Countries Clinical Trials Partnership","doi-asserted-by":"publisher","award":["IP.2007.3110.001"],"award-info":[{"award-number":["IP.2007.3110.001"]}],"id":[{"id":"10.13039\/501100001713","id-type":"DOI","asserted-by":"publisher"}]},{"name":"SIDA\/Sarec-Makerere Collaboration","award":["MakCHS_Malaria Subprogram"],"award-info":[{"award-number":["MakCHS_Malaria Subprogram"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Malar J"],"published-print":{"date-parts":[[2017,12]]},"DOI":"10.1186\/s12936-017-1970-1","type":"journal-article","created":{"date-parts":[[2017,8,9]],"date-time":"2017-08-09T10:56:51Z","timestamp":1502276211000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Prevalence of polymorphisms in glucose-6-phosphate dehydrogenase, sickle haemoglobin and nitric oxide synthase genes and their relationship with incidence of uncomplicated malaria in Iganga, Uganda"],"prefix":"10.1186","volume":"16","author":[{"given":"Catherine Nassozi","family":"Lwanira","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4981-6417","authenticated-orcid":false,"given":"Fred","family":"Kironde","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark","family":"Kaddumukasa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"G\u00f6te","family":"Swedberg","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2017,8,9]]},"reference":[{"key":"1970_CR1","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/ng.388","volume":"41","author":"M Jallow","year":"2009","unstructured":"Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, et al. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009;41:657\u201365.","journal-title":"Nat Genet"},{"key":"1970_CR2","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1038\/nature11334","volume":"489","author":"C Timmann","year":"2012","unstructured":"Timmann C, Thye T, Vens M, Evans J, May J, Ehmen C, et al. Genome-wide association study indicates two novel resistance loci for severe malaria. Nature. 2012;489:443\u20136.","journal-title":"Nature"},{"key":"1970_CR3","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1038\/ng.3107","volume":"46","author":"KA Rockett","year":"2014","unstructured":"Malaria Genomic Epidemiology Network, Rockett KA, Clarke GM, Fitzpatrick K, Hubbart C, Jeffreys AE, et al. Reappraisal of known malaria resistance loci in a large multicenter study. Nat Genet. 2014;46:1197\u2013204.","journal-title":"Nat Genet"},{"key":"1970_CR4","doi-asserted-by":"crossref","first-page":"2220","DOI":"10.1001\/jama.297.20.2220","volume":"297","author":"J May","year":"2007","unstructured":"May J, Evans JA, Timmann C, Ehmen C, Busch W, Thye T, et al. Hemoglobin variants and disease manifestations in severe falciparum malaria. JAMA. 2007;297:2220\u20136.","journal-title":"JAMA"},{"key":"1970_CR5","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1016\/S0140-6736(02)08273-9","volume":"359","author":"M Aidoo","year":"2002","unstructured":"Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002;359:1311\u20132.","journal-title":"Lancet"},{"key":"1970_CR6","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1038\/ng1660","volume":"37","author":"TN Williams","year":"2005","unstructured":"Williams TN, Mwangi TW, Wambua S, Peto TE, Weatherall DJ, Gupta S, et al. Negative epistasis between the malaria-protective effects of alpha+-thalassemia and the sickle cell trait. Nat Genet. 2005;37:1253\u20137.","journal-title":"Nat Genet"},{"key":"1970_CR7","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1086\/430744","volume":"192","author":"TN Williams","year":"2005","unstructured":"Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, et al. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis. 2005;192:178\u201386.","journal-title":"J Infect Dis"},{"key":"1970_CR8","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1086\/589778","volume":"198","author":"TD Clark","year":"2008","unstructured":"Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Staedke SG, et al. Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis. 2008;198:393\u2013400.","journal-title":"J Infect Dis"},{"key":"1970_CR9","doi-asserted-by":"crossref","first-page":"4551","DOI":"10.1182\/blood-2009-09-241844","volume":"115","author":"B Kreuels","year":"2010","unstructured":"Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, et al. Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Blood. 2010;115:4551\u20138.","journal-title":"Blood"},{"key":"1970_CR10","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1086\/592224","volume":"198","author":"PD Crompton","year":"2008","unstructured":"Crompton PD, Traore B, Kayentao K, Doumbo S, Ongoiba A, Diakite SA, et al. Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 2008;198:1265\u201375.","journal-title":"J Infect Dis"},{"key":"1970_CR11","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/S1473-3099(12)70055-5","volume":"12","author":"SM Taylor","year":"2012","unstructured":"Taylor SM, Parobek CM, Fairhurst RM. Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12:457\u201368.","journal-title":"Lancet Infect Dis"},{"key":"1970_CR12","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1186\/1475-2875-10-241","volume":"10","author":"N Carter","year":"2011","unstructured":"Carter N, Pamba A, Duparc S, Waitumbi JN. Frequency of glucose-6-phosphate dehydrogenase deficiency in malaria patients from six African countries enrolled in two randomized anti-malarial clinical trials. Malar J. 2011;10:241.","journal-title":"Malar J"},{"key":"1970_CR13","doi-asserted-by":"crossref","first-page":"15085","DOI":"10.7554\/eLife.15085","volume":"6","author":"GM Clarke","year":"2017","unstructured":"Clarke GM, Rockett K, Kivinen K, Hubbart C, Jeffreys AE, Rowlands K, et al. Characterisation of the opposing effects of G6PD deficiency on cerebral malaria and severe malarial anaemia. Elife. 2017;6:15085.","journal-title":"Elife"},{"key":"1970_CR14","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/S2352-3026(15)00152-0","volume":"2","author":"S Uyoga","year":"2015","unstructured":"Uyoga S, Ndila CM, Macharia AW, Nyutu G, Shah S, Peshu N, et al. Glucose-6-phosphate dehydrogenase deficiency and the risk of malaria and other diseases in children in Kenya: a case\u2013control and a cohort study. Lancet Haematol. 2015;2:437\u201344.","journal-title":"Lancet Haematol"},{"key":"1970_CR15","doi-asserted-by":"crossref","first-page":"1004960","DOI":"10.1371\/journal.pgen.1004960","volume":"11","author":"A Manjurano","year":"2015","unstructured":"Manjurano A, Sepulveda N, Nadjm B, Mtove G, Wangai H, Maxwell C, et al. African glucose-6-phosphate dehydrogenase alleles associated with protection from severe malaria in heterozygous females in Tanzania. PLoS Genet. 2015;11:1004960.","journal-title":"PLoS Genet"},{"key":"1970_CR16","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1371\/journal.pmed.0040066","volume":"4","author":"A Guindo","year":"2007","unstructured":"Guindo A, Fairhurst RM, Doumbo OK, Wellems TE, Diallo DA. X-linked G6PD deficiency protects hemizygous males but not heterozygous females against severe malaria. PLoS Med. 2007;4:66.","journal-title":"PLoS Med"},{"key":"1970_CR17","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/376246a0","volume":"376","author":"C Ruwende","year":"1995","unstructured":"Ruwende C, Khoo SC, Snow RW, Yates SN, Kwiatkowski D, Gupta S, et al. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature. 1995;376:246\u20139.","journal-title":"Nature"},{"key":"1970_CR18","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1038\/ejhg.2009.8","volume":"17","author":"TG Clark","year":"2009","unstructured":"Clark TG, Fry AE, Auburn S, Campino S, Diakite M, Green A, et al. Allelic heterogeneity of G6PD deficiency in West Africa and severe malaria susceptibility. Eur J Hum Genet. 2009;17:1080\u20135.","journal-title":"Eur J Hum Genet"},{"key":"1970_CR19","doi-asserted-by":"crossref","first-page":"43987","DOI":"10.1371\/journal.pone.0043987","volume":"7","author":"O Toure","year":"2012","unstructured":"Toure O, Konate S, Sissoko S, Niangaly A, Barry A, Sall AH, et al. Candidate polymorphisms and severe malaria in a Malian population. PLoS ONE. 2012;7:43987.","journal-title":"PLoS ONE"},{"key":"1970_CR20","doi-asserted-by":"crossref","first-page":"750","DOI":"10.4269\/ajtmh.2004.71.750","volume":"71","author":"S Parikh","year":"2004","unstructured":"Parikh S, Dorsey G, Rosenthal PJ. Host polymorphisms and the incidence of malaria in Ugandan children. Am J Trop Med Hyg. 2004;71:750\u20133.","journal-title":"Am J Trop Med Hyg"},{"key":"1970_CR21","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1038\/sj.gene.6363703","volume":"1","author":"F Migot-Nabias","year":"2000","unstructured":"Migot-Nabias F, Mombo LE, Luty AJ, Dubois B, Nabias R, Bisseye C, et al. Human genetic factors related to susceptibility to mild malaria in Gabon. Genes Immun. 2000;1:435\u201341.","journal-title":"Genes Immun"},{"key":"1970_CR22","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1086\/322037","volume":"184","author":"JF Kun","year":"2001","unstructured":"Kun JF, Mordmuller B, Perkins DJ, May J, Mercereau-Puijalon O, Alpers M, et al. Nitric oxide synthase 2 (Lambarene) (G\u2212954C), increased nitric oxide production, and protection against malaria. J Infect Dis. 2001;184:330\u20136.","journal-title":"J Infect Dis"},{"key":"1970_CR23","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1111\/j.1365-3156.2005.01438.x","volume":"10","author":"JP Cramer","year":"2005","unstructured":"Cramer JP, Nussler AK, Ehrhardt S, Burkhardt J, Otchwemah RN, Zanger P, et al. Age-dependent effect of plasma nitric oxide on parasite density in Ghanaian children with severe malaria. Trop Med Int Health. 2005;10:672\u201380.","journal-title":"Trop Med Int Health"},{"key":"1970_CR24","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1038\/nm1499","volume":"12","author":"I Gramaglia","year":"2006","unstructured":"Gramaglia I, Sobolewski P, Meays D, Contreras R, Nolan JP, Frangos JA, et al. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat Med. 2006;12:1417\u201322.","journal-title":"Nat Med"},{"key":"1970_CR25","doi-asserted-by":"crossref","first-page":"1651","DOI":"10.1016\/S0002-9440(10)64299-X","volume":"162","author":"S Serirom","year":"2003","unstructured":"Serirom S, Raharjo WH, Chotivanich K, Loareesuwan S, Kubes P, Ho M. Anti-adhesive effect of nitric oxide on Plasmodium falciparum cytoadherence under flow. Am J Pathol. 2003;162:1651\u201360.","journal-title":"Am J Pathol"},{"key":"1970_CR26","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1097\/QCO.0b013e32830ef5cf","volume":"21","author":"JB Weinberg","year":"2008","unstructured":"Weinberg JB, Lopansri BK, Mwaikambo E, Granger DL. Arginine, nitric oxide, carbon monoxide, and endothelial function in severe malaria. Curr Opin Infect Dis. 2008;21:468\u201375.","journal-title":"Curr Opin Infect Dis"},{"key":"1970_CR27","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s00439-009-0753-3","volume":"127","author":"MC Levesque","year":"2010","unstructured":"Levesque MC, Hobbs MR, O\u2019Loughlin CW, Chancellor JA, Chen Y, Tkachuk AN, et al. Malaria severity and human nitric oxide synthase type 2 (NOS2) promoter haplotypes. Hum Genet. 2010;127:163\u201382.","journal-title":"Hum Genet"},{"key":"1970_CR28","doi-asserted-by":"crossref","first-page":"186","DOI":"10.4269\/ajtmh.2003.68.186","volume":"68","author":"LE Mombo","year":"2003","unstructured":"Mombo LE, Ntoumi F, Bisseye C, Ossari S, Lu CY, Nagel RL, et al. Human genetic polymorphisms and asymptomatic Plasmodium falciparum malaria in Gabonese schoolchildren. Am J Trop Med Hyg. 2003;68:186\u201390.","journal-title":"Am J Trop Med Hyg"},{"key":"1970_CR29","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.actatropica.2011.11.004","volume":"121","author":"E Kamugisha","year":"2012","unstructured":"Kamugisha E, Bujila I, Lahdo M, Pello-Esso S, Minde M, Kongola G, et al. Large differences in prevalence of Pfcrt and Pfmdr1 mutations between Mwanza, Tanzania and Iganga, Uganda\u2014a reflection of differences in policies regarding withdrawal of chloroquine? Acta Trop. 2012;121:148\u201351.","journal-title":"Acta Trop"},{"key":"1970_CR30","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1186\/1756-0500-7-793","volume":"7","author":"M Kaddumukasa","year":"2014","unstructured":"Kaddumukasa M, Buwembo W, Sekikubo M, Naiwumbwe H, Namusoke F, Kiwuwa S, et al. Malariometric indices from Iganga, Uganda: baseline characterization in preparation of GMZ2 vaccine trial. BMC Res Notes. 2014;7:793.","journal-title":"BMC Res Notes"},{"key":"1970_CR31","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1186\/s12936-015-0875-0","volume":"14","author":"CN Lwanira","year":"2015","unstructured":"Lwanira CN, Kaddumukasa M, Swedberg G, Kironde F. Frequency of RANTES gene polymorphisms and their association with incidence of malaria: a longitudinal study on children in Iganga district, Uganda. Malar J. 2015;14:341.","journal-title":"Malar J"},{"key":"1970_CR32","unstructured":"Republic of Uganda. Uganda Clinical Guidelines: National guidelines on management of common conditions. Ministry of Health. 2010."},{"key":"1970_CR33","unstructured":"World Health Organization. World malaria report. Basic malaria microscopy part I learner\u2019s guide. 2nd ed. 1998. p. 74\u20135."},{"key":"1970_CR34","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1017\/PHN20062005","volume":"9","author":"M Onis de","year":"2006","unstructured":"de Onis M, Onyango AW, Borghi E, Garza C, Yang H, WHO Multicentre Growth Reference Study Group. Comparison of the World Health Organization (WHO) child growth standards and the National Center for Health Statistics\/WHO international growth reference: implications for child health programmes. Public Health Nutr. 2006;9:942\u20137.","journal-title":"Public Health Nutr"},{"key":"1970_CR35","doi-asserted-by":"crossref","first-page":"27077","DOI":"10.1371\/journal.pone.0027077","volume":"6","author":"Y Zhang","year":"2011","unstructured":"Zhang Y, Li C, Li K, Liu L, Jian Z, Gao T. Analysis of inducible nitric oxide synthase gene polymorphisms in vitiligo in Han Chinese people. PLoS ONE. 2011;6:27077.","journal-title":"PLoS ONE"},{"key":"1970_CR36","doi-asserted-by":"crossref","first-page":"17471","DOI":"10.1073\/pnas.0705390104","volume":"104","author":"JA Rowe","year":"2007","unstructured":"Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, Kone A, et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci USA. 2007;104:17471\u20136.","journal-title":"Proc Natl Acad Sci USA"},{"key":"1970_CR37","volume-title":"Generalisation of the Hardy\u2013Weinberg equation in the case of polygenic inheritance in population genetics and an estimation of the number of genes controlling human height","author":"V Balamurari","year":"2016","unstructured":"Balamurari V. Generalisation of the Hardy\u2013Weinberg equation in the case of polygenic inheritance in population genetics and an estimation of the number of genes controlling human height. Nugegoda: University of Sri Jayewardenepura; 2016."},{"key":"1970_CR38","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1128\/CDLI.11.1.29-34.2004","volume":"11","author":"ES Lugada","year":"2004","unstructured":"Lugada ES, Mermin J, Kaharuza F, Ulvestad E, Were W, Langeland N, et al. Population-based hematologic and immunologic reference values for a healthy Ugandan population. Clin Diagn Lab Immunol. 2004;11:29\u201334.","journal-title":"Clin Diagn Lab Immunol"},{"key":"1970_CR39","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/S2352-3026(15)00043-5","volume":"2","author":"TM Lopera-Mesa","year":"2015","unstructured":"Lopera-Mesa TM, Doumbia S, Konate D, Anderson JM, Doumbouya M, Keita AS, et al. Impact of red blood cell variants on childhood malaria in Mali: a prospective cohort study. Lancet Haematol. 2015;2:140\u20139.","journal-title":"Lancet Haematol"},{"key":"1970_CR40","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1186\/1475-2875-11-396","volume":"11","author":"EM Billig","year":"2012","unstructured":"Billig EM, McQueen PG, McKenzie FE. Foetal haemoglobin and the dynamics of paediatric malaria. Malar J. 2012;11:396.","journal-title":"Malar J"},{"key":"1970_CR41","doi-asserted-by":"crossref","first-page":"107965","DOI":"10.1371\/journal.pone.0107965","volume":"9","author":"DT Kangoye","year":"2014","unstructured":"Kangoye DT, Nebie I, Yaro JB, Debe S, Traore S, Ouedraogo O, et al. Plasmodium falciparum malaria in children aged 0\u20132\u00a0years: the role of foetal haemoglobin and maternal antibodies to two asexual malaria vaccine candidates (MSP3 and GLURP). PLoS ONE. 2014;9:107965.","journal-title":"PLoS ONE"},{"key":"1970_CR42","doi-asserted-by":"crossref","first-page":"0125929","DOI":"10.1371\/journal.pone.0125929","volume":"10","author":"BP Mmbando","year":"2015","unstructured":"Mmbando BP, Mgaya J, Cox SE, Mtatiro SN, Soka D, Rwezaula S, et al. Negative epistasis between sickle and foetal haemoglobin suggests a reduction in protection against malaria. PLoS ONE. 2015;10:0125929.","journal-title":"PLoS ONE"}],"container-title":["Malaria Journal"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12936-017-1970-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,10,14]],"date-time":"2020-10-14T16:02:01Z","timestamp":1602691321000},"score":1,"resource":{"primary":{"URL":"http:\/\/malariajournal.biomedcentral.com\/articles\/10.1186\/s12936-017-1970-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,8,9]]},"references-count":42,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2017,12]]}},"alternative-id":["1970"],"URL":"https:\/\/doi.org\/10.1186\/s12936-017-1970-1","relation":{},"ISSN":["1475-2875"],"issn-type":[{"value":"1475-2875","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,8,9]]},"article-number":"322"}}